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Population genetics and dynamics of Plasmodium falciparum: an ecological view

Published online by Cambridge University Press:  06 April 2009

K. P. Day ,
J. C. Koella ,
S. Nee ,
S. Gupta  and
A. F. Read
K. P. Day
Affiliation:
Department of Biology, Imperial College, London SW7 2BB, UK
J. C. Koella
Affiliation:
Department of Biology, Imperial College, London SW7 2BB, UK
S. Nee
Affiliation:
Zoology Department, University of Oxford, South Parks Road, Oxford OXI 3PS, UK
S. Gupta
Affiliation:
Department of Biology, Imperial College, London SW7 2BB, UK
A. F. Read
Affiliation:
Zoology Department, University of Oxford, South Parks Road, Oxford OXI 3PS, UK
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Summary

Molecular characterization of the Plasmodium falciparum genome has led to identification of polymorphic loci and the mechanisms generating genetic diversity in this parasite. This information has resulted in the development of molecular methods to type parasite diversity in the field. Consequently, we are now in a position to describe the population genetics and dynamics of P. falciparum. The limited number of field studies that have been conducted to date have revealed an extraordinary degree of genetic diversity in natural parasite populations. Heterozygous recombination which occurs during meiosis appears to be one mechanism for generating genetic diversity. The rate at which such recombination occurs in natural parasite populations defines the genetic structure of the parasite population and can influence the ability of the parasite to respond to selection pressure. The high frequency of single genotype infections and the female-biased gametocyte sex ratios found in hyperendemic malaria areas suggest that self-fertilization occurs frequently. Population- wide surveys of allele frequencies in endemic areas have, however, shown no evidence of linkage disequilibrium and are consistent with a panmictic population structure. We argue that these studies have only sampled symptomatic infections, within which rare or recombinant genotypes may be disproportionately represented. They also take no account of the spatial structure of P. falciparum populations. Systematic investigations of the amount of heterozygosity in small areas as part of population-wide surveys are required to define the genetic structure of P. falciparum populations. Population dynamic studies which consider genetic heterogeneity of P. falciparum have shown fluctuations of different serotypes in space and time. The host immune response appears to play an important role in generating these dynamics. Integrated field and laboratory studies, which consider the interaction between population genetics and dynamics, will be necessary to describe the population biology of P. falciparum.

Keywords

Plasmodium falciparummalariasexpanmixiaclonal theory.
Type
Malaria
Information
Parasitology , Volume 104 , Issue S1: Symposia of the British Society for Parasitology Volume 29:Human parasitic disease: the complementory roles of field and laboratory studies , June 1992 , pp. S35 - S52
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Allison, A. C. (1964). Polymorphism and natural selection in human populations. Cold Spring Harbor Symposium on Quantitative Biology 29, 137–49.CrossRefGoogle ScholarPubMed
Anders, R. F. (1986). Multiple cross-reactivities amongst antigens of Plasmodium falciparum impair the development of protective immunity against malaria. Parasite Immunology 8, 529–39.CrossRefGoogle ScholarPubMed
Anders, R. F. & Smythe, J. (1989). Polymorphic antigens in Plasmodium falciparum. Blood 74, 1865–75.CrossRefGoogle ScholarPubMed
Anders, R. F., Brown, G. V. & Edwards, A. E. (1983). Characterization of an S-antigen synthesized by several isolates of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 80, 6652–6.CrossRefGoogle ScholarPubMed
Arnot, D. (1989). Malaria and the major histocompatibility complex. Parasitology Today 5, 138–42.CrossRefGoogle ScholarPubMed
Aron, J. L. & May, R. M. (1982). The population dynamics of malaria. In The Population Dynamics of Infectious Diseases: Theory and Applications (ed. Anderson, R. M.), pp. 139–79. London: Chapman and Hall.CrossRefGoogle Scholar
Babiker, H. A., Creasey, A. M., Fenton, B., Bayoumi, H. A. L., Arnot, D. E. & Walliker, D. (1991). Genetic diversity of Plasmodium falciparum in a village in eastern Sudan. 1. Diversity of enzymes, 2D–PAGE proteins and antigens. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 572–7.CrossRefGoogle Scholar
Biggs, B. A., Gooze, L., Wycherley, K., Wollish, W., Southwell, B., Leech, J. H. & Brown, C. V. (1991). Antigenic variation in Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA (in the Press.)CrossRefGoogle ScholarPubMed
Boreham, P. F. L., Lenahan, J. K., Boulzaquet, R., Storey, J., Ashkar, T. S., Nambier, R. & Matsushima, T. (1979). Studies on multiple feeding by Anopheles gambiae s1. in Garki District, northern Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 418–23.CrossRefGoogle Scholar
Brown, K. N. (1990). The parasitology of malaria and the study of protective immunity. Immunology Letters 25, 97–100.CrossRefGoogle Scholar
Burkot, T. R., Craves, P. M., Paru, R. & Lagog, M. (1988). Mixed blood feeding by the malaria vectors in the Anopheles punctulatus complex (Diptera: Culicidae). Journal of Medical Entomology 25, 205–13.CrossRefGoogle ScholarPubMed
Carter, R. & McGregor, I. A. (1973). Enzyme variation in Plasmodium falciparum in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 830–7.CrossRefGoogle ScholarPubMed
Carter, R. & Voller, A. (1975). The distribution of enzyme variation in populations of Plasmodium falciparum in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 371–6.CrossRefGoogle ScholarPubMed
Cattani, J. A., Tulloch, J. L., Vebova, H., Jolley, D., Gibson, F. D., Moir, J. S., Heywood, P. F., Alpers, M. P., Stevenson, A. & Clancy, R. (1986). The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. American Journal of Tropical Medicine and Hygiene 35, 3–15.CrossRefGoogle Scholar
Charlwood, J. D., Graves, P. M. & Birley, M. H. (1986). Capture–recapture studies of Anopheles punctulatus Donitz (Diptera: Culicidae) from Papua New Guinea. Bulletin of Entomological Research 76, 211–27.CrossRefGoogle Scholar
Charnov, E. L. (1982). The Theory of Sex Allocation, Princeton: Princeton University Press.Google ScholarPubMed
Conway, D. J., Greenwood, B. M. & McBride, J. S. (1991). The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 103, 1–6.CrossRefGoogle ScholarPubMed
Conway, D. J. & McBRIDE, J. S. (1991 a). Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology 103, 7–16.CrossRefGoogle ScholarPubMed
Conway, D. J. & McBride, J. S. (1991 b). Genetic evidence for the importance of interrupted feeding by mosquitos in the transmission of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 454–6.CrossRefGoogle ScholarPubMed
Cowman, A. F., Saint, R. B., Coppel, R. L., Brown, G. V., Anders, R. F. & Kemp, D. J. (1985). Conserved sequences flank variable tandem repeats in two S-antigen genes of Plasmodium falciparum. Cell 40, 775–83.CrossRefGoogle ScholarPubMed
Cowman, A. F., Morry, M. J., Biggs, B. A., Cross, C. A. M. & Foote, S. J. (1988). Identification of amino acids linked to pyrimethamine resistance in dihydrofolate reductase thymidylate-synthase gene of Plassnodium falciparum. Proceedings of the National Academy of Sciences, USA 85, 9109–13.CrossRefGoogle Scholar
Creasey, A., Fenton, B., Walker, A., Thaithong, S., Oliveira, S., Mutambu, S. & Walliker, D. (1990). Genetic diversity of Plasmodium falciparum shows geographical variation. American Journal of Tropical Medicine and Hygiene 42, 403–13.CrossRefGoogle ScholarPubMed
Crow, J. F. & Kimura, M. (1962). The number of alleles that can be maintained in a finite population. Genetics 49, 725–38.Google Scholar
Dame, J. B., Williams, J. L., McCutchan, T. F., Weber, J. L., Wirtz, H., Hockmeyer, A., Maloy, W. T., Haynes, J. D., Schneider, I., Roberts, D., Sanders, C. S., Reddy, E. P., Diggs, C. L. & Miller, L. H. (1984). Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225, 593–9.CrossRefGoogle ScholarPubMed
Day, K. P. & Marsh, K. (1990). Naturally acquired immunity to Plasmodium falciparum. Parasitology Today 6, 68–71.Google Scholar
Dye, C. (1991). Population genetics of nonclonal, nonrandomly mating malaria parasites. Parasitology Today 7, 236–40.CrossRefGoogle ScholarPubMed
Flint, J., Hill, A. V. S., Bowden, D. K., Oppenheimer, S. J., Sill, P. H., Serjeantson, S. W., Bana-Koiri, J., Bhatla, K., Alpers, H. P., Boyce, A. J., Weatherall, D. J. & Clegg, J. B. (1986). High frequencies of α-thalassaemia are the result of natural selection by malaria. Nature, London 321, 744–50.CrossRefGoogle ScholarPubMed
Foote, S. J., Kyle, D. E., Martin, R. K., Oduola, A. M. J., Forsyth, K. P., Kemp, D. J. & Cowman, A. F. (1990). Several alleles of the multi-drug resistance gene are closely linked to chloroquine resistance in Plasmodium falciparum. Nature, London 345, 255–8.CrossRefGoogle ScholarPubMed
Forsyth, K. P., Philip, G., Smith, T., Klim, E., Southwell, B. & Brown, G. V. (1989 a). Diversity of antigens expressed on the surface of erythrocytes infected with mature Plasmodium falciparum parasites in Papua New Guinea. American Journal of Tropical Medicine and Hygiene 41, 259–65.CrossRefGoogle ScholarPubMed
Forsyth, K. P., Anders, R. F., Cattani, J. & Alpers, M. A. (1989 b). Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. American Journal of Tropical Medicine and Hygiene 40, 344–50.CrossRefGoogle ScholarPubMed
Frank, S. A. (1990). Sex allocation theory for birds and mammals. Annual Review of Ecology and Systematics 21, 13–55.CrossRefGoogle Scholar
Graves, P. M., Burkot, T. B., Carter, R., Cattani, J. A., Lagog, M., Parker, J., Brabin, B. J., Gibson, F. D., BRADLEY, D. J. & Alpers, M. A. (1988). Measurement of malarial infectivity of human populations to mosquitos in the Madang region, Papua New Guinea. Parasitology 96, 251–63.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1967). Extraordinary sex ratios. Science 156, 477–88.CrossRefGoogle ScholarPubMed
Herbert, P. D. N. (1987). The comparative evidence. In The Evolution of Sex and its Consequences (ed. Stearns, S. C.), pp. 192–4. Basel: Birkhäuser Verlag.Google Scholar
Hill, A. V. S., Allsopp, C. E. M., Kwiatkowski, D., Anstey, N. M., Twumasi, P., Rowe, P. A., Bennett, S., Brewster, D., McMichael, A. J. & Greenwood, B. M. (1991). Common West African HLA antigens are associated with protection from severe malaria. Nature, London 352, 595–600.CrossRefGoogle ScholarPubMed
Howard, R. J. (1988). Malarial proteins at the membrane of Plasmodium falciparum infected ervthrocytes and their involvement in cytoadherence to endothelial cells. Progress in Allergy 41, 98–147.Google ScholarPubMed
Joshi, H., Subbarao, S. K., Raghavendra, K. & Sharma, V. P. (1989). Plasmodium vivax: enzyme polymorphism in isolates of Indian origin. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 179–81.CrossRefGoogle ScholarPubMed
Kemp, D. J., Cowman, A. F. & Walliker, D. (1990). Genetic diversity in Plasmodium falciparum. Advances in Parasitology 29, 75–149.CrossRefGoogle ScholarPubMed
Koella, J. C. (1991). On the use of mathematical models of malaria transmission. Acta Tropica 49, 1–25.CrossRefGoogle ScholarPubMed
Lockyer, M. J. & Schwartz, R. T. (1987). Strain variation in the circumsporozoite gene of Plasmodium falciparum. Molecular and Biochemical Parasitology 22, 101–8.CrossRefGoogle ScholarPubMed
McBride, J. S., Walliker, D. & Morgan, G. (1985). Antigenic diversity in the human malaria parasite Plasmodium falciparum. Science 217, 254–7.CrossRefGoogle Scholar
McConkey, G. A., Waters, A. P. & McCutchan, T. F. (1990). The generation of genetic diversity in malaria parasites. Annual Review of Microbiology 44, 479–98.CrossRefGoogle ScholarPubMed
McCutchan, T. S. & Waters, A. P. (1990). Mutations with multiple independent origins in surface antigens mark the targets of biological selection pressures. Immunology Letters 25, 23–6.CrossRefGoogle Scholar
MacDonald, G. (1957). The Epidemiology and Control of Malaria. London: Oxford University Press.Google Scholar
Marsh, K. & Howard, R. J. (1986). Antigens induced in the circumsporozoite gene of Plasmodium falciparum: expression of diverse and Conserved determinants. Science 231, 150–3.CrossRefGoogle Scholar
Marsh, K., Otoo, L., Hayes, R. J., Carson, D. C. & Greenwood, B. M. (1989). Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 293–303.CrossRefGoogle ScholarPubMed
Pascala, S. W., Hassell, M. P. & May, R. M. (1990). Host–parasite associations in patchy environments. Nature, London 344, 150–3.CrossRefGoogle Scholar
Peterson, D., Walliker, D. & Wellems, T. (1988 a). Evidence that a point mutation in dihydro-folate reductase thymidylate synthase gene confers pyrimethamine resistance in falciparum malaria. Proceedings of the National Academy of Sciences, USA 85, 9114–18.CrossRefGoogle Scholar
Peterson, M. G., Coppel, R. L., McIntyre, P., Langford, C. J., Woodrow, G., Brown, G. V., Anders, R. F. & Kemp, D. J. (1988 b). Variation in the precursor to the major merozoite surface antigens of Plasmodium falciparum. Molecular and Biochemical Parasitology 27, 291–302.CrossRefGoogle Scholar
Port, G. R., Boreham, P. F. L. & Bryan, J. H. (1980). The relationship of host size to feeding of mosquitos of the Anopheles gambiae Giles complex (Diptera: CuliCidae). Bulletin of Entomological Research 70, 133–44.CrossRefGoogle Scholar
Ranford-Cartwright, L. C., Balfe, P., Carter, R. & Walliker, D. (1991). Genetic hybrids of Plasmodium falciparum identified by amplification of genomic DNA from single oocysts. Molecular and Biochemical Parasitology 49, 239–44.CrossRefGoogle ScholarPubMed
Read, A. F., Narara, A., Nee, S., Keymer, A. E. & Day, K. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, (in the Press).CrossRefGoogle ScholarPubMed
Rosenberg, R., Wirtz, R. A., Schneider, I. & Burge, H. (1990). An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 209–12.CrossRefGoogle ScholarPubMed
Ross, R. (1911). The Prevention of Malaria. London: Murray.Google ScholarPubMed
Sadun, E. H., Hickman, R. L., Welloe, B. T., Moon, A. D. & Udeozo, I. D. R. (1966). Active and passive immunization of chimpanzees infected with West African and Southeast Asian strains of Plasmodium falciparum. Military Medicine 131 (Suppl.), 1250–62.CrossRefGoogle ScholarPubMed
Saul, A., Myler, P., Schofield, L. & Kidson, C. (1984). A high molecular weight antigen in Plasmodium falciparum recognised by inhibitory monoclonal antibodies. Parasite Immunology 6, 39.CrossRefGoogle ScholarPubMed
Scherf, A., Mattel, D. & Southou, J. L. (1991). Multiple infections and unusual distribution of block 2 of MSA I gene of Plasmodium falciparum detected in West African clinical isolates by polymerase chain reaction analysis. Molecular and Biochemical Parasitology 44, 297–300.CrossRefGoogle Scholar
Schoen, D. J. & Brown, A. H. D. (1991). Intraspecific variation in population gene diversity and effective population size correlates with mating system in plants. Proceedings of the National Academy of Sciences, USA 88, 4494–7.CrossRefGoogle ScholarPubMed
Smythe, J. A., Coppel, R. L., Day, K. P., Martin, R. K., Oduola, A. M. J., Kemp, D. J. & Anders, R. F. (1991). Structural diversity in the Plasmodium falciparum merozoite surface antigen 2. Proceedings of the National Academy of Sciences, USA 88, 1751–5.CrossRefGoogle ScholarPubMed
Snewin, V. A., England, S. M., Sims, P. F. G. & Hyde, J. E. (1989). Characterization of the dihydrofolate reductase thymidylate synthetase gene from human malaria parasites highly resistant to pyrirnethamine. Gene 76, 41–52.CrossRefGoogle Scholar
Tanabe, K., MacKay, M., Goman, M. & Scaife, J. G. (1987). Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 195, 273–87.CrossRefGoogle Scholar
Thaithong, S., Sueblinwong, T. & Beale, G. H. (1981). Enzyme typing of some isolates of Plasmodium falciparum from Thailand. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 268–70.CrossRefGoogle ScholarPubMed
Tibayrenc, M. & Ayala, F. J. (1991). Towards a population genetics of micro-organisms: the clonal theory of parasitic protozoa. Parasitology Today 7, 228–32.CrossRefGoogle Scholar
Tibayrenc, M., Kjellberg, F., Arnaud, J., Oury, B., Breniere, S. F., Darde, M. L. & Ayala, F. J. (1991). Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proceedings of the National Academy of Sciences, USA 88, 5129–33.CrossRefGoogle ScholarPubMed
Tibayrenc, M., Kjellberg, F. & Ayala, F. J. (1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Plasmodium, Trichomonas and Trypanosoma and their medical and taxonomic consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–18.CrossRefGoogle Scholar
Walliker, D. (1991). Malaria parasites: randomly interbreeding or ‘clonal’ populations? Parasitology Today 7, 232–5.CrossRefGoogle ScholarPubMed
Walliker, D., Quakyi, L. A., Wellems, T. E., McCutchan, T. F., Szarfman, A., London, W. T., Corcoran, L. M., Burkot, T. R. & Carter, R. (1987). Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236, 1661–6.CrossRefGoogle ScholarPubMed
Wellems, T. E., Walker-Jonah, A. & Panton, L. J. (1991). Genetic mapping of the chloroquine-resistance locus on Plasmodium falciparum chromosome 7. Proceedings of the National Academy of Sciences, USA 88, 3382–6.CrossRefGoogle ScholarPubMed
Wilson, R. J. M., McGregor, I. A. & Hall, P. J. (1975). Persistence and recurrence of S-antigens in Plasmodium falciparum infections in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 461–7.Google ScholarPubMed
Wilson, R. J. M., McGregor, I. A., Hall, P., Williams, K. & Bartholomew, R. (1969). Antigens associated with Plasmodium falciparum infections in man. Lancet ii, 201–5.CrossRefGoogle Scholar